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Homogeneous Nuclear Background for Mitochondrial Cline in Northern Range of Notochthamalus Scabrosus

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Homogeneous Nuclear Background for Mitochondrial Cline in Northern Range of Notochthamalus Scabrosus INVESTIGATION Homogeneous Nuclear Background for Mitochondrial Cline in Northern Range of Notochthamalus scabrosus Christina Zakas,* Ken Jones,† and John P. Wares‡,1 *New York University, Center for Genomics and Systems Biology, New York, New York 10003, †University of Colorado, Aurora, Colorado 80045, and ‡University of Georgia, Athens, Georgia 30602 ABSTRACT A mitochondrial cline along the Chilean coast in the barnacle Notochthamalus scabrosus KEYWORDS suggests a species history of transient allopatry and secondary contact. However, previous studies of RAD-seq nuclear sequence divergence suggested population genetic homogeneity across northern and central SNP Chile. Here, we collect single-nucleotide polymorphism data from pooled population samples sequenced cytonuclear with restriction site2associated DNA sequencing procedures, confirm these data with the use of a Golden- disequilibrium Gate array, and identify a discordance between population genetic patterns in the nuclear and mitochon- barnacle drial genomes. This discordance was noted in previous work on this species, but here it is confirmed that the Chile nuclear genome exhibits only slight phylogeographic variation across 3000 km of coastline, in the presence of a strong and statistically significant mitochondrial cline. There are nevertheless markers (approximately 5% of nuclear single-nucleotide polymorphisms) exhibiting cytonuclear disequilibrium relative to mitotype. Although these data confirm our previous explorations of this species, it is likely that some of the nuclear genomic diversity of this species has yet to be explored, as comparison with other barnacle phylogeography studies suggest that a divergence of similar magnitude should be found in the nuclear genome somewhere else in the species range. Patterns of mitochondrial diversity have heralded great discoveries in Pavlova et al. 2013). For example, divergence of mitochondrial lin- biodiversity and often are used to indicate the likelihood that evolu- eages in an Australian robin (Eopsaltria australis) exhibits an east- tionarily distinct lineages are harbored within recognized morpholog- west pattern, perpendicular to the latitudinal structure of nuclear ical species (Hebert et al. 2004; Moritz and Cicero 2004). However, markers (Pavlova et al. 2013). divergence of mitochondrial lineages is not necessarily representative of Another such case of discordance has been identified in the the rest of a eukaryotic genome (Hudson and Coyne 2002; Hickerson barnacle Notochthamalus scabrosus (Foster and Newman 1987) along et al. 2006). In some cases, exploration of divergence at nuclear the central coast of Chile (Zakas et al. 2009). Two divergent mito- markers supports a general pattern (Tellier et al. 2009), but in other chondrial lineages are found in this species, with one of them only cases the two genomic compartments appear to have wildly distinct found in natural populations south of ~30°S(Zakaset al. 2009; Laughlin histories of isolation and/or selection (Toews and Brelsford 2012; et al. 2012). A nuclear gene (elongation factor 1-a; nEF1) surveyed for the same region showed no such geographic pattern of genetic fi Copyright © 2014 Zakas et al. diversi cation (Zakas et al. 2009), despite the capacity for this gene doi: 10.1534/g3.113.008383 region to mirror such patterns and magnitudes of divergence in Manuscript received September 9, 2013; accepted for publication November 25, other coastal barnacles (Sotka et al. 2004). Because the nEF1 data 2013; published Early Online December 17, 2013. did not exhibit the expected genealogical divergence, as seen in other This is an open-access article distributed under the terms of the Creative Commons Attribution Unported License (http://creativecommons.org/licenses/ barnacle species with similar mitochondrial clines (Sotka et al. by/3.0/), which permits unrestricted use, distribution, and reproduction in any 2004), it is clear that a better representation of diversity and diver- medium, provided the original work is properly cited. gence in the nuclear genome will be needed to understand the Supporting information is available online at http://www.g3journal.org/lookup/ phylogeography of N. scabrosus. suppl/doi:10.1534/g3.113.008383/-/DC1. Such a result suggests a discordant history for the mitochondrial Data from this article are available NCBI BioProject under PRJNA227359. 1Corresponding author: Department of Genetics, University of Georgia, Athens, GA and nuclear genomes of N. scabrosus, but of course one nuclear locus 30602. E-mail: [email protected] is not sufficiently representative of the dynamics of the genome. Volume 4 | February 2014 | 225 Recent advances in DNA sequencing technology (Schuster 2008) for individuals comprised solely of the A1, A2 (“northern”), and B make it readily possible to efficiently survey a larger fraction of the (“southern”) mitochondrial haplotypes as described in Laughlin genome for population genetic analysis. Elucidating the pattern of et al. (2012). population divergence by the use of many thousands of nuclear loci Pooled genomic DNA were cut per standard protocols (Peterson reveals the potential combinations of ecological and evolutionary et al. 2012) by the use of SpeI and Sau3AI, chosen for their utility in forces that drive this mismatch in genome histories. Here we use similar projects (K. Jones, unpublished results). Libraries were then a combination of reduced-representation genome sequencing (restric- prepared for Illumina sequencing by the use of TruSeq adapters and tion site2associated DNA sequencing, or RADseq; Peterson et al. 100-bp paired ends were sequenced on an Illumina HiSequation 2500 2012) of population samples and direct multilocus genotyping of at the University of Colorado at Denver core facility. markers developed from such data to find nuclear regions that may be associated with the divergent mitochondrial lineages found in Genome-wide single-nucleotide polymorphism N. scabrosus. Because the aforementioned nEF1 data did not exhibit (SNP) analysis a cline, we were interested in determining the extent to which a large RADseq data were trimmed to remove adapter sequence and error- representation of the nuclear genome displayed a concordant pattern. prone regions. Sequence fragments were aligned and organized with We also assess the utility of pooled RADseq data by comparison with the program STACKS (Catchen et al. 2013). Because these data rep- direct genotyping of individuals in a subset of populations; the op- resent pooled samples from distinct locations, the consensus stacks portunity to collect appropriate data via pooled sampling, if it provides were used as the reference library in the program POPOOLATION2 (Kofler fi results consistent with individual genotypes, could be an ef cient and et al. 2011), which aligns reads from pooled libraries to these reference inexpensive way to identify genome-wide diversity in nonmodel sequences and generates allele frequency and other population genetic organisms. statistics such as FST. SNPs were only included for analysis with a minimum fragment coverage of 50 and minimum quality score of 20. METHODS Specimen collection and sequencing SNP selection Collected specimens and DNA isolation protocols are described in To genotype at the individual level, SNPs were chosen for assay using detail in Laughlin et al. (2012). Sample locations are shown in Figure 1. the Illumina BeadXPress platform as in Zakas and Wares (2012). Pooled samples of each location, with separate pools for “low” and Thus, SNPs were identified that had sequenced flanking regions of “high” intertidal samples from Temblador and Guanaqueros, were .30 bp for primer design; these were scored by Illumina for their generated for each site with equimolar concentrations of each in- probability of success. Only SNPs with the greatest possible quality dividual. All individuals included had been previously sequenced at ranking were selected for further analysis. We chose 192 for multi- mitochondrial cytochrome oxidase I (COI) and identified to mito- locus genotyping, setting specific aprioricriteria for selection follow- chondrial type. Three separate genomic DNA pools were generated ing Zakas et al. (2012), where ribosomal markers were eliminated and a balance of SNPs from coding regions and anonymous regions, as well as apparent nonsynonymous polymorphisms and synonymous polymorphisms were chosen. Consensus sequences for each region were evaluated with NCBI BLAST; any contig that blasted to a mito- chondrial region with score e , 0.001 was considered a likely mito- chondrial region and was excluded. We further screened the SNP library for potential outliers that exhibit high FST values among locations using the program BAYESSCAN (Foll and Gaggiotti 2008); these outliers were included in the BeadX- Press assay. To minimize potential ascertainment biases in selection of SNPs for completion of the array, SNPs with minor allele frequencies of 0.3020.35, 0.3620.40, 0.4120.45, and 0.4620.50 were equally represented. Markers with lower minor allele frequencies were elim- inated to guard against sequencing artifacts as in Zakas et al. (2012). Further, only one SNP was selected from each identified sequence “stack” (contig) for the BeadXPress array to minimize linkage disequi- librium among markers. BeadXPress assay data Genomic DNA samples at 20250 ng/mL for individuals from three representative locations (Arica, Las Cruces, and Niebla; Figure 1) were prepared by the Georgia Genomics Facility and run on a BeadXPress platform
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